The evolution of photosynthesis

Julian Hibberd, Cambridge University

The process of photosynthesis goes back over 3 billion years. But in just the last 30 million years or so, a new and dramatically better form of photosynthesis has appeared. But it requires a considerable number of changes within plant structures to sustain it. What Cambridge Plant Scientist Julian Hibberd wanted to know was, in what order (if any) these changes needed to have a curd to make this so-called C4 photosynthesis feasible.

Julian - Photosynthesis is the synthesises the mechanism by which almost all life on this planet is maintained because it’s the system by which CO2 is converted into sugars and carbohydrates. It provides our basic food stuff. Historically, it provides our fuel because a lot of fossil fuels were laid down by ancient plants. And so, we’re interested in ho

w a particular flavour of photosynthesis evolved about 30 million years ago because it’s actually more efficient than the ancestral version of photosynthesis.

Chris - So, tell us about the two types of photosynthesis. What are they and how do the differ?

Julian - The ancestral version of photosynthesis we think evolved in bacteria about 3.6 billion years ago and that uses an enzyme which affects the CO2 into sugars. That enzyme never have to distinguish between the CO2 molecule that now uses an oxygen which is now present in the atmosphere. The reason for that was, those ancient bacteria went in an atmosphere with oxygen, but later on, some more complex bacteria evolved which started to pump oxygen out into the atmosphere. As a consequence, the photosynthetic organisms today have to distinguish between carbon dioxide CO2 and oxygen. At the molecular level, they are actually quite similar. And so, this poor protein which is meant to fix CO2 some other time makes mistakes and uses oxygen instead.

Chris - That presumably reduces the efficiency of the process.

Julian - Yeah and the efficiency is reduced the most in the tropics and subtropics because there's a correlation between the specificity of the protein and its ability to fix CO2. As you get warmer, it fixes CO2 less efficiently.

Chris - So, how did evolution tackle that?

Julian - So, evolution has tackled it actually on many occasions.

In the land plants, we think at least 60 different lineages of land plants evolved the derived version of photosynthesis that I work on and there are other lineages which have evolved other mechanisms to cut to concentrate carbon dioxide around this photosynthetic protein. We’ve become interested in how – what is actually a really complicated trait kind of evolved so many times and the evidence at the moment is it’s over 60.

Chris - When this trait evolved, what sorts of things have had to change?

Julian - In a C4 leaf, there are changes to the structure of the leaf itself, to the leaf anatomy. There are changes to structures within the cell. So, cell biology changes and there are also really distinct changes to gene

expression and the spatial arrangement to photosynthesis within those cells in the leaf. So, it’s really quite a complicated suite of alternations which have to occur.

Chris - Your question is, in what order did those things crop up? Excuse the plant pun.

Julian - Exactly. So, we’re interested in whether specific traits occur early along that evolutionary path to see for photosynthesis or late or actually, whether they can be flexible, whether they can occur in some lineages very early on and some lineages much later on. But you still get to the final phenotype at the end.

Chris - So, how did you do this?

Julian - What we did was we took about 73 different plant species. Some of which used the ancestral C3 version of photosynthesis. Some used this derived C4 version of photosynthesis. Some remarkably which have characteristics of both of those types of photosynthesis but without the full syndrome. We mapped onto those species which trait were visible in each. And so, we characterise them as either having a set of 16 C3 traits. So, that species was completely C3, completely ancestral in terms of photosynthesis or another species might have 16 C4 traits. So, it will be completely derived. In the intermediate species, we’d have a mixture of some C3 and some C4 traits.

Chris - I suppose if you look at the evolutionary timeline separating the ones which are fully C4 and those that are fully C3, you can ask, where along that timeline some of these traits must've occurred.

Julian - Exactly. So, we’ve estimated that some traitsare very likely to occur early on in the transition from C3 to C4 photosynthesis and conversely, some always come in at the end. But there are a few which seem to be bimodal. So, they have different distributions. Sometimes they come in late and sometimes they come in early which implies that there are many flexible routes for a plant – a photosynthetic organism – to move from this ancestral version of photosynthesis to this more efficient derived version of photosynthesis.

Chris - Putting all of your findings together, what then is the bottom line?

Julian - So, what we discovered was that this complex system which has evolved multiple times is likely to have evolved multiple times because there are many ways of getting to the same end point. So, ‘many roads lead to Rome’ I think is a phrase which could be used to describe our system. This very complicated version of photosynthesis seems to have got there on multiple occasions because there are many ways to reach that final goal. The other thing that we infer from our results is that the initial environmental drivers for evolution of C4 photosynthesis is unlikely to have actually been improvements in photosynthesis itself, but more likely to have been changes in the ability of the plants to use relatively low water supplies or something like that.

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